Chapter 14 : How Biofilms Evade Host Defenses

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

How Biofilms Evade Host Defenses, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap14-1.gif /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap14-2.gif


Historically, microbial organisms have been grown in pure liquid cultures as free-floating “planktonic” cells, promoting the general theory of the unicellular lifestyle. However, in the late 1970s, Costerton et al. ( ) demonstrated that groups of bacteria were embedded in a highly hydrated polysaccharide matrix that mediated adhesion to solid aquatic surfaces. Several years later, the same research team called these cellular communities “biofilms,” defined as a functionally heterogeneous aggregate of microcolonies or single cells encased in a matrix of self-produced extracellular polymeric molecules that could adhere either to organic, abiotic surfaces or to each other ( ). Microbial biofilms can develop into highly organized structures containing channels in which water, nutrients, and metabolic waste can be transported. Adhesion to substrates or surfaces induces expression of a large number of genes, while cell aggregates in different regions in a biofilm exhibit different gene expression profiles that regulate biofilm development and maturation processes ( ). A large amount of research since the 1980s has brought to light the theory that most, if not all, bacteria and fungi can form biofilms as a survival mechanism in hostile environments, providing protection from biotic and abiotic stresses ( ). Prime candidates for cell attachment and biofilm growth are surfaces exposed to or containing moisture and some nutrients. Natural or man-made substrates for cell attachment and biofilm growth include river stones, oil and gas installations, ship hulls, water pipes, food-processing surfaces, contaminated surgical instruments, indwelling medical devices, human teeth, and infected wounds ( ). In this chapter, we will present an overview of the life cycle of biofilms and their diversity, detection methods for biofilm development, and host immune responses to pathogens. We will then focus on current concepts in bacterial and fungal biofilm immune evasion mechanisms.

Citation: Roilides E, Simitsopoulou M, Katragkou A, Walsh T. 2015. How Biofilms Evade Host Defenses, p 287-300. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0012-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Costerton JW,, Geesey GG,, Cheng KJ . 1978. How bacteria stick. Sci Am 238 : 86 95.[PubMed] [CrossRef]
2. Costerton JW,, Lewandowski Z,, Caldwell DE,, Korber DR,, Lappin-Scott HM . 1995. Microbial biofilms. Annu Rev Microbiol 49 : 711 745.[PubMed] [CrossRef]
3. Costerton JW,, Stewart PS,, Greenberg EP . 1999. Bacterial biofilms: a common cause of persistent infections. Science 284 : 1318 1322.[PubMed] [CrossRef]
4. Donlan RM,, Costerton JW . 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15 : 167 193.[CrossRef]
5. Mack D,, Becker P,, Chatterjee I,, Dobinsky S,, Knobloch JK,, Peters G,, Rohde H,, Herrmann M . 2004. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 294 : 203 212.[PubMed] [CrossRef]
6. Ramage G,, Mowat E,, Jones B,, Williams C,, Lopez-Ribot J . 2009. Our current understanding of fungal biofilms. Crit Rev Microbiol 35 : 340 355.[PubMed] [CrossRef]
7. Wei Q,, Ma LZ . 2013. Biofilm matrix and its regulation in Pseudomonas aeruginosa . Int J Mol Sci 14 : 20983 21005.[PubMed] [CrossRef]
8. Palkova Z,, Vachova L . 2006. Life within a community: benefit to yeast long-term survival. FEMS Microbiol Rev 30 : 806 824.[PubMed] [CrossRef]
9. Donlan RM . 2001. Biofilms and device-associated infections. Emerg Infect Dis 7 : 277 281.[PubMed] [CrossRef]
10. Salta M,, Wharton JA,, Blache Y,, Stokes KR,, Briand JF . 2013. Marine biofilms on artificial surfaces: structure and dynamics. Environ Microbiol. [Epub ahead of print.] doi:10.1111/1462-2920.12186. [PubMed] [CrossRef]
11. Abdallah M,, Benoliel C,, Drider D,, Dhulster P,, Chihib NE . 2014. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch Microbiol. [Epub ahead of print.] doi:10.1007/s00203-014-0983-1. [CrossRef]
12. Otto M . 2008. Staphylococcal biofilms. Curr Top Microbiol Immunol 322 : 207 228.[PubMed] [CrossRef]
13. Fey PD,, Olson ME . 2010. Current concepts in biofilm formation of Staphylococcus epidermidis . Future Microbiol 5 : 917 933.[PubMed] [CrossRef]
14. Moorthy S,, Watnick PI . 2004. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol Microbiol 52 : 573 587.[PubMed] [CrossRef]
15. Caiazza NC,, Merritt JH,, Brothers KM,, O’Toole GA . 2007. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189 : 3603 3612.[PubMed] [CrossRef]
16. Walsh TJ,, Schlegel R,, Moody M,, Costerton JW,, Salcman M . 1986. Ventriculo-atrial shunt infection due to Cryptococcus neoformans: an ultrastructural and quantitative microbiological study. Neurosurgery 18 : 373 375.[PubMed] [CrossRef]
17. Martinez LR,, Casadevall A . 2005. Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect Immun 73 : 6350 6362.[PubMed] [CrossRef]
18. Zhao X,, Oh SH,, Yeater KM,, Hoyer LL . 2005. Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 151 : 1619 1630.[PubMed] [CrossRef]
19. Castano I,, Pan SJ,, Zupancic M,, Hennequin C,, Dujon B,, Cormack BP . 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata . Mol Microbiol 55 : 1246 1258.[PubMed] [CrossRef]
20. Hornby JM,, Jensen EC,, Lisec AD,, Tasto JJ,, Jahnke B,, Shoemaker R,, Dussault P,, Nickerson KW . 2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67 : 2982 2992.[PubMed] [CrossRef]
21. Davey ME,, Caiazza NC,, O’Toole GA . 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185 : 1027 1036.[PubMed] [CrossRef]
22. Rajendran R,, Williams C,, Lappin DF,, Millington O,, Martins M,, Ramage G . 2013. Extracellular DNA release acts as an antifungal resistance mechanism in mature Aspergillus fumigatus biofilms. Eukaryot Cell 12 : 420 429.[PubMed] [CrossRef]
23. Shopova I,, Bruns S,, Thywissen A,, Kniemeyer O,, Brakhage AA,, Hillmann F . 2013. Extrinsic extracellular DNA leads to biofilm formation and colocalizes with matrix polysaccharides in the human pathogenic fungus Aspergillus fumigatus . Front Microbiol 4 : 141. [PubMed] [CrossRef]
24. Krappmann S,, Ramage G . 2013. A sticky situation: extracellular DNA shapes Aspergillus fumigatus biofilms. Front Microbiol 4 : 159. [PubMed] [CrossRef]
25. Uppuluri P,, Chaturvedi AK,, Srinivasan A,, Banerjee M,, Ramasubramaniam AK,, Kohler JR,, Kadosh D,, Lopez-Ribot JL . 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6 : e1000828. doi:10.1371/journal.ppat.1000828. [CrossRef]
26. Wang R,, Khan BA,, Cheung GY,, Bach TH,, Jameson-Lee M,, Kong KF,, Queck SY,, Otto M . 2011. Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J Clin Invest 121 : 238 248.[PubMed] [CrossRef]
27. Periasamy S,, Joo HS,, Duong AC,, Bach TH,, Tan VY,, Chatterjee SS,, Cheung GY,, Otto M . 2012. How Staphylococcus aureus biofilms develop their characteristic structure. Proc Natl Acad Sci USA 109 : 1281 1286.[PubMed] [CrossRef]
28. Harriott MM,, Noverr MC . 2009. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53 : 3914 3922.[PubMed] [CrossRef]
29. Demuyser L,, Jabra-Rizk MA,, Van Dijck P . 2014. Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms. Pathog Dis 70 : 219 230.[PubMed] [CrossRef]
30. Shirtliff ME,, Peters BM,, Jabra-Rizk MA . 2009. Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 299 : 1 8.[PubMed] [CrossRef]
31. Peters BM,, Jabra-Rizk MA,, Scheper MA,, Leid JG,, Costerton JW,, Shirtliff ME . 2010. Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59 : 493 503.[PubMed] [CrossRef]
32. Wolcott R,, Costerton JW,, Raoult D,, Cutler SJ . 2013. The polymicrobial nature of biofilm infection. Clin Microbiol Infect 19 : 107 112.[PubMed] [CrossRef]
33. Mowat E,, Rajendran R,, Williams C,, McCulloch E,, Jones B,, Lang S,, Ramage G . 2010. Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett 313 : 96 102.[PubMed] [CrossRef]
34. Christensen GD,, Simpson WA,, Younger JJ,, Baddour LM,, Barrett FF,, Melton DM,, Beachey EH . 1985. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22 : 996 1006.[PubMed]
35. Chandra J,, Kuhn DM,, Mukherjee PK,, Hoyer LL,, McCormick T,, Ghannoum MA . 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183 : 5385 5394.[PubMed] [CrossRef]
36. Hassan A,, Usman J,, Kaleem F,, Omair M,, Khalid A,, Iqbal M . 2011. Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis 15 : 305 311.[PubMed] [CrossRef]
37. Taff HT,, Nett JE,, Andes DR . 2012. Comparative analysis of Candida biofilm quantitation assays. Med Mycol 50 : 214 218.[PubMed] [CrossRef]
38. Mowat E,, Butcher J,, Lang S,, Williams C,, Ramage G . 2007. Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus . J Med Microbiol 56 : 1205 1212.[PubMed] [CrossRef]
39. Sontakke S,, Cadenas MB,, Maggi RG,, Diniz PP,, Breitschwerdt EB . 2009. Use of broad range 16S rDNA PCR in clinical microbiology. J Microbiol Methods 76 : 217 225.[PubMed] [CrossRef]
40. Pontes DS,, Lima-Bittencourt CI,, Chartone-Souza E,, Amaral Nascimento AM . 2007. Molecular approaches: advantages and artifacts in assessing bacterial diversity. J Ind Microbiol Biotechnol 34 : 463 473.[PubMed] [CrossRef]
41. Rhoads DD,, Wolcott RD,, Sun Y,, Dowd SE . 2012. Comparison of culture and molecular identification of bacteria in chronic wounds. Int J Mol Sci 13 : 2535 2550.[PubMed] [CrossRef]
42. Banchereau J,, Briere F,, Caux C,, Davoust J,, Lebecque S,, Liu YJ,, Pulendran B,, Palucka K . 2000. Immunobiology of dendritic cells. Annu Rev Immunol 18 : 767 811.[PubMed] [CrossRef]
43. Gantner BN,, Simmons RM,, Canavera SJ,, Akira S,, Underhill DM . 2003. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197 : 1107 1117.[PubMed] [CrossRef]
44. Romani L . 2011. Immunity to fungal infections. Nat Rev Immunol 11 : 275 288.[PubMed] [CrossRef]
45. Norrby-Teglund A,, Johansson L . 2013. Beyond the traditional immune response: bacterial interaction with phagocytic cells. Int J Antimicrob Agents 42( Suppl) : S13 S16.[PubMed] [CrossRef]
46. Singh PK,, Parsek MR,, Greenberg EP,, Welsh MJ . 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417 : 552 555.[PubMed] [CrossRef]
47. Overhage J,, Campisano A,, Bains M,, Torfs EC,, Rehm BH,, Hancock RE . 2008. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect Immun 76 : 4176 4182.[PubMed] [CrossRef]
48. Britigan BE,, Hayek MB,, Doebbeling BN,, Fick RB Jr . 1993. Transferrin and lactoferrin undergo proteolytic cleavage in the Pseudomonas aeruginosa-infected lungs of patients with cystic fibrosis. Infect Immun 61 : 5049 5055.[PubMed]
49. Schmidtchen A,, Frick IM,, Andersson E,, Tapper H,, Bjorck L . 2002. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol Microbiol 46 : 157 168.[PubMed] [CrossRef]
50. Jensen PO,, Givskov M,, Bjarnsholt T,, Moser C . 2010. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol 59 : 292 305.[PubMed] [CrossRef]
51. Meyle E,, Stroh P,, Gunther F,, Hoppy-Tichy T,, Wagner C,, Hansch GM . 2010. Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. Int J Artif Organs 33 : 608 620.[PubMed]
52. Gunther F,, Wabnitz GH,, Stroh P,, Prior B,, Obst U,, Samstag Y,, Wagner C,, Hansch GM . 2009. Host defense against Staphylococcus aureus biofilms infection: phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol Immunol 46 : 1805 1813.[PubMed] [CrossRef]
53. Meyle E,, Brenner-Weiss G,, Obst U,, Prior B,, Hansch GM . 2012. Immune defense against S. epidermidis biofilms: components of the extracellular polymeric substance activate distinct bactericidal mechanisms of phagocytic cells. Int J Artif Organs 35 : 700 712.[PubMed] [CrossRef]
54. Chandra J,, McCormick TS,, Imamura Y,, Mukherjee PK,, Ghannoum MA . 2007. Interaction of Candida albicans with adherent human peripheral blood mononuclear cells increases C. albicans biofilm formation and results in differential expression of pro- and anti-inflammatory cytokines. Infect Immun 75 : 2612 2620.[PubMed] [CrossRef]
55. Katragkou A,, Kruhlak MJ,, Simitsopoulou M,, Chatzimoschou A,, Taparkou A,, Cotten CJ,, Paliogianni F,, Diza-Mataftsi E,, Tsantali C,, Walsh TJ,, Roilides E . 2010. Interactions between human phagocytes and Candida albicans biofilms alone and in combination with antifungal agents. J Infect Dis 201 : 1941 1949.[PubMed] [CrossRef]
56. Martinez LR,, Casadevall A . 2006. Cryptococcus neoformans cells in biofilms are less susceptible than planktonic cells to antimicrobial molecules produced by the innate immune system. Infect Immun 74 : 6118 6123.[PubMed] [CrossRef]
57. Archer NK,, Mazaitis MJ,, Costerton JW,, Leid JG,, Powers ME,, Shirtliff ME . 2011. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence 2 : 445 459.[PubMed] [CrossRef]
58. Leid JG,, Shirtliff ME,, Costerton JW,, Stoodley P . 2002. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 70 : 6339 6345.[PubMed] [CrossRef]
59. Guenther F,, Stroh P,, Wagner C,, Obst U,, Hansch GM . 2009. Phagocytosis of staphylococci biofilms by polymorphonuclear neutrophils: S. aureus and S. epidermidis differ with regard to their susceptibility towards the host defense. Int J Artif Organs 32 : 565 573.[PubMed]
60. Thurlow LR,, Hanke ML,, Fritz T,, Angle A,, Aldrich A,, Williams SH,, Engebretsen IL,, Bayles KW,, Horswill AR,, Kielian T . 2011. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo . J Immunol 186 : 6585 6596.[PubMed] [CrossRef]
61. Stroh P,, Gunther F,, Meyle E,, Prior B,, Wagner C,, Hansch GM . 2011. Host defense against Staphylococcus aureus biofilms by polymorphonuclear neutrophils: oxygen radical production but not phagocytosis depends on opsonisation with immunoglobulin G. Immunobiology 216 : 351 357.[PubMed] [CrossRef]
62. Cerca N,, Jefferson KK,, Oliveira R,, Pier GB,, Azeredo J . 2006. Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun 74 : 4849 4855.[PubMed] [CrossRef]
63. Hanke ML,, Kielian T . 2012. Deciphering mechanisms of staphylococcal biofilm evasion of host immunity. Front Cell Infect Microbiol 2 : 62. [PubMed] [CrossRef]
64. Hanke ML,, Heim CE,, Angle A,, Sanderson SD,, Kielian T . 2013. Targeting macrophage activation for the prevention and treatment of Staphylococcus aureus biofilm infections. J Immunol 190 : 2159 2168.[PubMed] [CrossRef]
65. Alhede M,, Bjarnsholt T,, Givskov M,, Alhede M . 2014. Pseudomonas aeruginosa biofilms: mechanisms of immune evasion. Adv Appl Microbiol 86 : 1 40.[PubMed] [CrossRef]
66. Jensen ET,, Kharazmi A,, Lam K,, Costerton JW,, Hoiby N . 1990. Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 58 : 2383 2385.[PubMed]
67. Jesaitis AJ,, Franklin MJ,, Berglund D,, Sasaki M,, Lord CI,, Bleazard JB,, Duffy JE,, Beyenal H,, Lewandowski Z . 2003. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 171 : 4329 4339.[PubMed] [CrossRef]
68. Bjarnsholt T,, Jensen PO,, Burmolle M,, Hentzer M,, Haagensen JA,, Hougen HP,, Calum H,, Madsen KG,, Moser C,, Molin S,, Hoiby N,, Givskov M . 2005. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151 : 373 383.[PubMed] [CrossRef]
69. Walker TS,, Tomlin KL,, Worthen GS,, Poch KR,, Lieber JG,, Saavedra MT,, Fessler MB,, Malcolm KC,, Vasil ML,, Nick JA . 2005. Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73 : 3693 3701.[PubMed] [CrossRef]
70. Parks QM,, Young RL,, Poch KR,, Malcolm KC,, Vasil ML,, Nick JA . 2009. Neutrophil enhancement of Pseudomonas aeruginosa biofilm development: human F-actin and DNA as targets for therapy. J Med Microbiol 58 : 492 502.[PubMed] [CrossRef]
71. Watt AP,, Courtney J,, Moore J,, Ennis M,, Elborn JS . 2005. Neutrophil cell death, activation and bacterial infection in cystic fibrosis. Thorax 60 : 659 664.[PubMed] [CrossRef]
72. Leid JG,, Willson CJ,, Shirtliff ME,, Hassett DJ,, Parsek MR,, Jeffers AK . 2005. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 175 : 7512 7518.[PubMed] [CrossRef]
73. Jensen ET,, Kharazmi A,, Hoiby N,, Costerton JW . 1992. Some bacterial parameters influencing the neutrophil oxidative burst response to Pseudomonas aeruginosa biofilms. APMIS 100 : 727 733.[PubMed] [CrossRef]
74. Jensen PO,, Bjarnsholt T,, Phipps R,, Rasmussen TB,, Calum H,, Christoffersen L,, Moser C,, Williams P,, Pressler T,, Givskov M,, Hoiby N . 2007. Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa . Microbiology 153 : 1329 1338.[PubMed] [CrossRef]
75. Alhede M,, Bjarnsholt T,, Jensen PO,, Phipps RK,, Moser C,, Christophersen L,, Christensen LD,, van Gennip M,, Parsek M,, Hoiby N,, Rasmussen TB,, Givskov M . 2009. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155 : 3500 3508.[PubMed] [CrossRef]
76. Van Gennip M,, Christensen LD,, Alhede M,, Phipps R,, Jensen PO,, Christophersen L,, Pamp SJ,, Moser C,, Mikkelsen PJ,, Koh AY,, Tolker-Nielsen T,, Pier GB,, Hoiby N,, Givskov M,, Bjarnsholt T . 2009. Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS 117 : 537 546.[PubMed] [CrossRef]
77. Roilides E,, Walsh T . 2004. Recombinant cytokines in augmentation and immunomodulation of host defenses against Candida spp. Med Mycol 42 : 1 13.[PubMed] [CrossRef]
78. Xie Z,, Thompson A,, Sobue T,, Kashleva H,, Xu H,, Vasilakos J,, Dongari-Bagtzoglou A . 2012. Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing. J Infect Dis 206 : 1936 1945.[PubMed] [CrossRef]
79. Katragkou A,, Simitsopoulou M,, Chatzimoschou A,, Georgiadou E,, Walsh TJ,, Roilides E . 2011. Effects of interferon-gamma and granulocyte colony-stimulating factor on antifungal activity of human polymorphonuclear neutrophils against Candida albicans grown as biofilms or planktonic cells. Cytokine 55 : 330 334.[PubMed] [CrossRef]
80. Nett J,, Lincoln L,, Marchillo K,, Andes D . 2007. Beta -1,3 glucan as a test for central venous catheter biofilm infection. J Infect Dis 195 : 1705 1712.[PubMed] [CrossRef]
81. Dongari-Bagtzoglou A,, Kashleva H,, Dwivedi P,, Diaz P,, Vasilakos J . 2009. Characterization of mucosal Candida albicans biofilms. PLoS One 4 : e7967. doi:10.1371/journal.pone.0007967. [PubMed] [CrossRef]
82. Al-Fattani MA,, Douglas LJ . 2006. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55 : 999 1008.[PubMed] [CrossRef]
83. Luo G,, Ibrahim AS,, Spellberg B,, Nobile CJ,, Mitchell AP,, Fu Y . 2010. Candida albicans Hyr1p confers resistance to neutrophil killing and is a potential vaccine target. J Infect Dis 201 : 1718 1728.[PubMed] [CrossRef]
84. Giard JC,, Riboulet E,, Verneuil N,, Sanguinetti M,, Auffray Y,, Hartke A . 2006. Characterization of Ers, a PrfA-like regulator of Enterococcus faecalis . FEMS Immunol Med Microbiol 46 : 410 418.[PubMed] [CrossRef]
85. Gentry-Weeks CR,, Karkhoff-Schweizer R,, Pikis A,, Estay M,, Keith JM . 1999. Survival of Enterococcus faecalis in mouse peritoneal macrophages. Infect Immun 67 : 2160 2165.[PubMed]
86. Daw K,, Baghdayan AS,, Awasthi S,, Shankar N . 2012. Biofilm and planktonic Enterococcus faecalis elicit different responses from host phagocytes in vitro . FEMS Immunol Med Microbiol 65 : 270 282.[PubMed] [CrossRef]
87. Mathew S,, Yaw-Chyn L,, Kishen A . 2010. Immunogenic potential of Enterococcus faecalis biofilm under simulated growth conditions. J Endod 36 : 832 836.[PubMed] [CrossRef]
88. Chotirmall SH,, McElvaney NG . 2014. Fungi in the cystic fibrosis lung: bystanders or pathogens? Int J Biochem Cell Biol 52 : 161 173.[PubMed] [CrossRef]
89. Roilides E,, Simitsopoulou M . 2010. Local innate host response and filamentous fungi in patients with cystic fibrosis. Med Mycol 48( Suppl 1) : S22 S31.[PubMed] [CrossRef]
90. Tasina E,, Simitsopoulou M,, Roilides E . 2012. The innate immune response to filamentous fungi in patients with cystic fibrosis. CML Cystic Fibrosis 2 : 29 39.
91. Kreindler JL,, Steele C,, Nguyen N,, Chan YR,, Pilewski JM,, Alcorn JF,, Vyas YM,, Aujla SJ,, Finelli P,, Blanchard M,, Zeigler SF,, Logar A,, Hartigan E,, Kurs-Lasky M,, Rockette H,, Ray A,, Kolls JK . 2010. Vitamin D3 attenuates Th2 responses to Aspergillus fumigatus mounted by CD4+ T cells from cystic fibrosis patients with allergic bronchopulmonary aspergillosis. J Clin Invest 120 : 3242 3254.[PubMed] [CrossRef]
92. Nett J,, Andes D . 2006. Candida albicans biofilm development, modeling a host-pathogen interaction. Curr Opin Microbiol 9 : 340 345.[PubMed] [CrossRef]


Generic image for table

Steps in the biofilm growth cycle

Citation: Roilides E, Simitsopoulou M, Katragkou A, Walsh T. 2015. How Biofilms Evade Host Defenses, p 287-300. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0012-2014
Generic image for table

Methods for biofilm detection and quantitation

Citation: Roilides E, Simitsopoulou M, Katragkou A, Walsh T. 2015. How Biofilms Evade Host Defenses, p 287-300. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0012-2014
Generic image for table

Relation of innate host defenses and specific microbial biofilms

Citation: Roilides E, Simitsopoulou M, Katragkou A, Walsh T. 2015. How Biofilms Evade Host Defenses, p 287-300. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0012-2014

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error